• CLINICAL RESEARCH •
Effects of exercise on lipid metabolism and musculoskeletal
fitness in female athletes
Kung-Tung Chen, Rong-Sen Yang
Kung-Tung Chen, Department of Genenal Education, Ming Hsin (186.44±24.90 mg/dL vs 193.00±23.48 mg/dL) were higher,
University of Science and Technology, Hsinchu 304, Taiwan, China but the HDL was significantly lower (62.18±10.68 mg/dL
Rong-Sen Yang, Department of Orthopaedics, College of Medicine, vs 52.26±4.84 mg/dL, P<0.05) in postmenopausal athletes
National Taiwan University, Taipei 10043, Taiwan, China (5/36) group than in postmenopausal control group (9/30).
Supported by the National Science Council of Taiwan, NSC91-2413-
H-159-001
Correspondence to: Dr. Rong-Sen Yang, Department of Orthopaedics, CONCLUSION: Postmenopausal athletes (5/36) who no
National Taiwan University Hospital, No.7 Chung-Shan South Road, longer took competing exercises had reduced levels of
Taipei 10043, Taiwan, China. yang@ha.mc.ntu.edu.tw physical activity, faced increased risk of cardiovascular
Telephone: +886-2-2312-3456 Ext 3958 Fax: +886-2-23936577 disease compared to active athletes (31/36) and the
Received: 2003-10-16 Accepted: 2003-11-20 postmenopausal controls (9/30). We may thus concluded
that long term exercise effectively improves musculoskeletal
fitness and prevents BMD loss in female athletes.
Abstract
Chen KT, Yang RS. Effects of exercise on lipid metabolism and
AIM: This study investigated the effects of intense training musculoskeletal fitness in female athletes. World J Gastroenterol
on lipid metabolism, bone metabolism and bone mineral 2004; 10(1): 122-126
density (BMD) in female athletes. http://www.wjgnet.com/1007-9327/10/122.asp
have shown them to predict bone mass changes[3-16]. measured using an EIA kit obtained from Metra Biosystems
Therefore, the purpose of this study was to explore the (Monutain View, CA, USA). Urine Dpd level was measured
physiological function of female athletes, including BMD, renal using enzyme immunoassay (Ciba-Corning ACS-180) kits
function, liver function, hormone status, bone marker assay, purchased from Bayer international (Bayer Diagnostics,
lipid metabolism and muscle biology related to the effectiveness Tarrytown, NY, USA).
of exercise intervention for the health status of female athletes
compared with controls. BMD determination
Calcaneus site BMD was measured via speed of sound (SOS)
MATERIALS AND METHODS equipped for a bone mineral densitometry (Aloka Medical Ltd,
modelAOS-100, Tokyo, Japan) and all BMD values were also
Subjects expressed as a T-score, accurately reflecting the BMD. Distal site
Sixty-six female subjects participated in this investigation, with BMD was measured using the osmometer DTX-100 (SPA, Single
ages ranging between 18 and 55 yrs. The sample group was Photon Absorptiometry, Osmometer, Rodovre, Denmark). The
the athlete group (n=36), while the control group comprised scanners were calibrated daily against the standard calibration
non-athletic individuals (n=30). Inclusion criteria were that block supplied by the manufacturer to control baseline drift.
the female athletes had participated in high-intensity resistance
or impact activities (e.g., basketball, dancing). Exclusion Statistical analysis
criteria for both the subjects and the controls were that the All data were analysed, using SPSS 10.0 software, and were
subjects had no major medical illnesses, including coronary presented as mean rank statistical difference, using the Kurskal-
artery disease which could influence lipid metabolism, and Wallis (K-W) test. After that the non-parameter statistics were
were free of other risk factors that are associated with be used. The confidence interval was set at 95% and the
influencing lipid metabolism, such as smoking or ethanol intake significance level used was K<0.05 (two sides). All statistical
or treatment within the last two years with systemic gluco- analyses were carried out with SPSS statistical package. The
mineralocorticoids, anticonvulsants, bisphosphonates, Kruskal-Wallis test does not use any information on the relative
oestrogen, or raloxifene. Five athletes competed with national magnitude of each observation when compared with every other
level (5/36) and nine non-athletic subjects (9/30) were included observation in the combined sample. This comparison is replaced
in the analysis of postmenopausal women. The parameters to in each observation by its rank in the pool sample. The smallest
be measured included body composition, radius BMD and observation is replaced by its rank 1, the next smallest by rank
calcaneus BMD, lung function, muscular endurance, renal 2, and so on, the largest by its rank n. Since the test is an
function, liver function and hormone status. extension of the Mann-Whitney-Wilcoxon (M-W-W) test.
Either K value or P value below 0.05 is considered significant.
Anthropometric measurement of body composition
Anthropometric measurements were taken based on conventional
criteria. The measurement procedures of body weight (Wt) RESULTS
and body height (Ht) were estimated to the nearest 0.1 kg and No difference in body composition
0.5 cm, respectively. Finally BMI was calculated using the The thirty-six female athletes enrolled in this cross- sectional
formula: BMI (kg/m2)=Wt (kg)/Ht (m2). study did not differ significantly in terms of BF, BF%, BMI
and resistance compared with the control group (Table 1).
Health related fitness
They were tested using a modified Guthrie R test[6]. Health Table 1 Body composition of two groups
related fitness tests included vertical jump, 3 min steps, sit-
reach, hand grip and 1 min sit-ups items. 66 females
in the control group. However, LDL (105.93±30.76 mg/dL vs Table 4 Serum enzyme activities related to renal and liver
102.89±25.92 mg/dL), TG (81.53±49.53 mg/dL vs 74.60±48.31 metabolism
mg/dL) and CHO (170.20±32.20 mg/dL vs 168.06±28.13 mg/dL)
were lower in the athlete group than those of the control group. Group n ALP Cre ALB DBIL
Thus exercise could improve the lipid metabolism, and it is
good for health. Control group (mean rank) 30 27.07 27.88 27.77 27.65
Athlete group (mean rank) 36 38.86ac 38.18ab 38.28a 38.38a
Table 3 No significant differences in blood CHO and lipid
variables between both groups a
K<0.05 vs statistically significant when compared with con-
trol group. bP<0.05 vs statistically significant when compared
Group n HDL LDL CHO TG Hb with control group. cP<0.01 vs statistically significant when
compared with control group.
Control group 30 31.92 34.65 34.92 35.02 28.75
(mean rank)
Athlete group 36 34.82 32.54 32.32 32.24 37.46
Renal and liver function
Table 4 shows that no difference between the data (data not
(mean rank)
shown here) of the two groups in terms of blood enzymes such
Table 2 Muscular strength and endurance assessment among controls and athlete groups
Group n Sit-reach 1 min sit-ups Vertical jump Hand grip 3 min steps Vital capacity
Control group (mean rank) 30 22.18 22.05 22.23 31.27 29.60 30.58
Athlete group (mean rank) 36 42.93ab 43.04ab 42.89ab 35.36 36.75 35.93
a
K<0.001 vs statistically significant when compared with control group. bP<0.001 vs statistically significant when compared with
control group.
a
K<0.05 vs statistically significant when compared with control group. bK<0.01 vs statistically significant when compared with
control group. cK<0.001 vs statistically significant when compared with control group. dP<0.05 vs statistically significant when
compared with control group.
Table 6 Hormonal findings in athletes with significance by non-parameter statistics test compared with controls
Control group (mean rank) 30 32.28 25.78 31.77 36.43 31.37 35.65
Athletes group (mean rank) 36 34.51 39.93ab 34.94 31.06 35.28 31.71
a
K<0.01 vs statistically significant when compared with control group. bP<0.01 vs statistically significant when compared with
control group.
Table 7 Biochemical bone turnover markers and BMD in athletes with significance by non-parameter statistics test as compared
with controls
Control group (mean rank) 30 25.87 27.23 25.72 20.10 28.38 26.23
Athletes group (mean rank) 36 39.86be 38.72ad 39.99b 43.83cf 37.76a 39.56b
a
K<0.05 vs statistically significant when compared with control group. bK<0.01 vs statistically significant when compared with
control group. cK<0.001 vs statistically significant when compared with control group. dP<0.05 vs statistically significant when
compared with control group. eP<0.01 vs statistically significant when compared with control group. fP<0.001 vs statistically
significant when compared with control group.
Table 8 Postmenopausal female athlete lipid metabolism compared to premenopausal active athletes
Premenopausal (mean rank) 31 16.84 17.08 20.15 16.74 16.98 16.55 18.79
Postmenopausal (mean rank) 5 28.60ac 27.30be 8.30ac 29.40ad 27.90ac 30.60b 16.70
a
K<0.05 vs statistically significant when compared with premenopausal group. bK<0.01 vs statistically significant when com-
pared with premenopausal group. cP<0.05 vs statistically significant when compared with premenopausal group. dP<0.01 vs
statistically significant when compared with premenopausal group. eP<0.001 vs statistically significant when compared with
premenopausal group.
Chen KT et al. Lipid metabolism and musculoskeletal fitness in female athletes 125
as glutamic oxalocetic transminase (GOT), glutamic pyruvic Lipid metabolism in postmenopausal females
transminase (GPT), blood urea nitrogen (BUN), uric acid (UA), Results from this study show higher levels of TG (90.22±39.82
total protein (TP), globulin (GLO) and bilirubin (BIL). But mg/dL vs 147.00±87.21 mg/dL), CHO (186.44±24.90 mg/dL
the control group displayed significantly lower alkaline vs 193.00±23.48 mg/dL), but lower levels of HDL (62.18±10.68
phosphatase (ALP) (61.03±13.99 U/L vs 70.81±15.23 U/L, mg/dL vs 52.26±4.84 mg/dL, P<0.05), Hb (13.82±0.88 g/dL
K<0.05, P<0.01), ALB (4.52±0.18 g/dL vs 4.62±0.27 g/dL, vs 13.52±0.21 g/dL) in postmenopausal athletes (5/36) group
K<0.05), Cre (0.75±0.09 mg/dL vs 0.81±0.10 mg/dL, P<0.05, compared with the postmenopausal control group (9/30). This
K<0.05) and direct bilirubin (DBIL) (0.25±1.11 mg/dL vs implies that the effect is a cardiovascular disease risk for
0.29±0.8 mg/dL, K<0.05) than the athlete group. postmenopausal retired female athletes (Table 9).
CHO (K<0.05, P<0.05), TG (K<0.01) compared to the 8 Hendriksen IJ, Meeuwsen T. The effect of intermittent training
premenopausal active athletes (31/36). Postmenopausal retired in hypobaric hypoxia on sea-level exercise: a cross-over study in
female athletes (5/36) engaged in less physical activity than humans. Eur J Appl Physiol 2003; 88: 396-403
previously, displayed increase rates of liver and renal dysfunction, 9 Williams CD, Dobridge JD, Meyer WR, Hackney AC. Effects of
the route of estrogen administration and exercise on hormonal
which require further investigation[17,23-28].
levels in postmenopausal women. Fertil Steril 2002; 77: 1118-1124
An understanding of the dyslipidemia and ensuing 10 Leelawattana R, Ziambaras K, Roodman WJ, Lyss C, Wagner D,
atherosclerosis has implications for the pathophysiology of Klug T, Armamento VR, Civitelli R. The oxidative metabolism
coronary heart disease (CHD). Risk of cardiac morbidity and of estradiol conditions postmenopausal bone density and bone
mortality is directly related to concentration of plasma total loss. J Bone Miner Res 2000; 15: 2513-2520
CHO or LDL. Lipid lowering therapy has been shown to reduce 11 Deschenes MR, Kraemer WJ. Performance and physiologic adap-
the risk of cardiovascular events in both high risk individuals tations to resistance training. Am J Phys Med Rehabil 2002; 81: S3-16
and patients with manifest CHD[17-22,24-28]. The present study 12 Hayashi T, Ito I, Kano H, Endo H, Iguchi A. Estriol (E3) replace-
has found that postmenopausal retired female athletes (5/36) ment improves endothelial function and bone mineral density in
who were no longer engaged in strenuous physical activity, very elderly women. J Gerontol A Biol Sci Med Sci 2000; 55: 183-190
13 Hou MF, Lin SB, Yuan SS, Tsai LY, Tsai SM, Hsieh JS, Huang TJ.
they had a significantly higher BF% (K<0.05, P<0.001) and
Diagnostic value of urine deoxypyridinoline for detecting bone
BMI (K<0.05, P<0.001) compared to the active female athletes metastases in breast cancer patients. Ann Clin Lab Sci 2003; 33: 55-61
(31/36) group, specifically, in lipid dysfunction marker with 14 Miller CJ, Dunn EV, Thomas EJ, Sankarankutty M. Urinary free
the postmenopausal retired female athletes. Results from this deoxypyridinoline excretion in lactating and non-lactating Ara-
study show higher levels of TG, CHO, but lower levels of HDL, bic women of the United Arab Emirates. Ann Clin Biochem 2003;
Hb in athletes (5/36) group compared with the control group 40: 394-397
(9/30). Then, five postmenopausal athletes (5/36), who had 15 Ormarsdottir S, Ljunggren O, Mallmin H, Olofsson H, Blum WF,
retired from competition, and were engaged in less physical Loof L. Circulating levels of insulin-like growth factors and their
activity than previously, had significantly higher BF%, BMI binding proteins in patients with chronic liver disease: Lack of
and lipid dysfunction markers had a significantly decreased correlation with bone mineral density. Liver 2001; 21: 123-128
16 Wu LY, Yang TC, Kuo SW, Hsiao CF, Hung YJ, Hsieh CH, Tseng
level of HDL (P<0.05) compared to the controls (9/30). This
HC, Hsieh AT, Chen TW, Chang JB, Pei D. Correlation between
suggest that the effect is a cardiovascular disease risk for bone mineral density and plasma lipids in Taiwan. Endocrine Res
postmenopausal retired female athletes. 2003; 29: 317-319
Future studies should recruit more numbers of female 17 Huang TH, Lin SC, Chang FL, Hsieh SS, Liu SH, Yang RS. Effects of
athletes, who have retired from competition but still maintained different exercise modes on mineralization, structure, and biomechani-
high levels of physical activity, and then compare this group cal properties of growing bone. J Appl Physiol 2003; 95: 300-307
with the low physical activity group that serves as the control 18 Tsauo JY, Chien MY, Yang RS. Spinal performance and func-
group. Lipid metabolism related apolipoprotein E (ApoE) tional impairment in postmenopausal women with osteoporosis
genotypes with an allele specific oligonucleotide (ASO) based and osteopenia without vertebral fracture. Osteoporos Int 2002;
microarray system may interact with exercise training to affect 13: 456-460
19 Huang TH, Yang RS, Hsieh SS, Liu SH. Effects of caffeine and exercise
their plasma lipid profiles. To clarify the atherogenic risk of
on the development of bone: a densitometric and histomorphometric
different lipoprotein phenotypes, the relations among total study in young Wistar rats. Bone 2002; 30: 293-299
CHO, LDL, HDL and CHD risk in older female athletes should 20 Hui SL, Perkins AJ, Zhou L, Longcope C, Econs MJ, Peacock M,
be investigated. McClintock C, Johnston CC Jr. Bone loss at the femoral neck in
premenopausal white women: effects of weight change and sex-
hormone levels. J Clin Endocrinol Metab 2002; 87: 1539-1543
ACKNOWLEDGEMENTS
21 Prestwood KM, Kenny AM, Kleppinger A, Kulldorff M.
We are grateful to Li-Shin Hospital in Taoyuan County, Taiwan Ultralow-dose micronized 17beta-estradiol and bone density and
that provided all laboratory tests in this study, which helped bone metabolism in older women: a randomized controlled trial.
us to complete the research subjects. JAMA 2003; 290: 1042-1048
22 van den Beld AW, de Jong FH, Grobbee DE, Pols HA, Lamberts
SW. Measures of bioavailable serum testosterone and estradiol
REFERENCES and their relationships with muscle strength, bone density, and
1 Huuskonen J, Vaisanen SB, Kroger H, Jurvelin JS, Alhava E, body composition in elderly men. J Clin Endocrinol Metab 2000;
Rauramaa R. Regular physical exercise and bone mineral density: 85: 3276-3282
a four-year controlled randomized trial in middle-aged men. The 23 Guichelaar MM, Malinchoc M, Sibonga J, Clarke BL, Hay JE.
DNASCO study. Osteoporos Int 2001; 12: 349-355 Bone metabolism in advanced cholestatic liver disease: analysis
2 Humphries B, Newton RU, Bronks R, Marshall S, McBride J, by bone histomorphometry. Hepatology 2002; 36: 895-903
Triplett MT, Hakkinen K, Kraemer WJ, Humphries N. Effect of 24 Fan JG, Zhong L, Xu ZJ, Tia LY, Ding XD, Li MS, Wang GL.
exercise intensity on bone density, strength, and calcium turn- Effects of low-calorie diet on steatohepatitis in rats with obesity
over in older women. Med Sci Sports Exerc 2000; 32: 1043-1050 and hyperlipidemia. World J Gastroenterol 2003; 9: 2045-2049
3 Wolff I, van Croonenborg JJ, Kemper HC, Kostense PJ, Twisk 25 Lu LG, Zeng MD, Li JQ, Hua J, Fan JG, Fan ZP, Qiu DK. Effects
JW. The effect of exercise training programs on bone mass: a meta- of lipid on proliferation and activation of rat hepatic stellate cells
analysis of published controlled trials in pre- and postmenopausal (I). World J Gastroenterol 1998; 4: 497-499
women. Osteoporos Int 1999; 9: 1-12 26 Wakatsuki A, Okatani Y, Ikenoue N, Shinohara K, Watanabe K,
4 Karlsson MK. Skeletal effects of exercise in men. Calcif Tissue Int Fukaya T. Effect of lower dose of oral conjugated equine estrogen
2001; 69: 196-199 on size and oxidative susceptibility of low-density lipoprotein par-
5 Pettersson U, Nordstrom P, Lorentzon R. A comparison of bone ticles in postmenopausal women. Circulation 2003; 108: 808-813
mineral density and muscle strength in young male adults with 27 Tanko LB, Bagger YZ, Nielsen SB, Christiansen C. Does serum
different exercise level. Calcif Tissue Int 1999; 64: 490-498 cholesterol contribute to vertebral bone loss in postmenopausal
6 Guthrie R. The use of medical examinations for employment women? Bone 2003; 32: 8-14
purposes. J Law Med 2003; 11: 93-102 28 Chen BY, Wei JG, Wang YC, Wang CM, Yu J, Yang XX. Effects of
7 Kraemer WJ, Ratamess NA, French DN. Resistance training for cholesterol on the phenotype of rabbit bile duct fibroblasts. World
health and performance. Curr Sports Med Rep 2002; 1: 165-171 J Gastroenterol 2003; 9: 351-355
Edited by Wang XL